Closely related Symbiodinium spp. differ in relative dominance in coral reef host communities across environmental, latitudinal and biogeographic gradients

The diversity and community structures of symbiotic dinoflagellates are described from reef invertebrates in southern and central provinces of the Great Barrier Reef (GBR), Australia, and Zamami Island, Okinawa, Japan. The symbiont assemblages from region to region were dominated by Clade C Symbiodinium spp. and consisted of numerous host-specific and/or rare types (specialists), and several types common to many hosts (generalists). Prevalence in the host community among certain host-generalist symbionts differed between inshore and offshore environments, across latitudinal (central versus southern GBR) gradients, and over wide geographic ranges (GBR versus Okinawa). One particular symbiont (C3h) from the GBR had a dramatic shift in dominance. Its prevalence ranged from being extremely rare, or absent on high-latitude reefs to dominating the scleractinian diversity on a mid-latitude inshore reef. These changes occurred among coral fauna whose larvae must acquire symbionts from environmental sources (horizontal symbiont acquisition). Such differences did not occur among 'vertical transmitters' such as Porites spp., Montipora spp. and pocilloporids (corals that directly transmit symbionts to their offspring) or among those hosts displaying 'horizontal acquisition', but that associate with specific symbionts. Most host-specialized types were found to be characteristic of a particular geographic region (i.e. Okinawa versus Central GBR versus Southern GBR). The mode of symbiont acquisition may play an important role in how symbiont composition may shift in west Pacific host communities in response to climate change. There is no indication that recent episodes of mass bleaching have provoked changes in host-symbiont combinations from the central GBR.

Photosynthate translocation increases in response to low seawater pH in a coral-dinoflagellate symbiosis

This study has examined the effect of low seawater pH values (induced by an increased CO2 partial pressure) on the rates of photosynthesis, as well as on the carbon budget and carbon translocation in the scleractinian coral species Stylophora pistillata, using a new model based on 13C labelling of the photosynthetic products. Symbiont photosynthesis contributes to a large part of the carbon acquisition in tropical coral species, and it is thus important to know how environmental changes affect this carbon acquisition and allocation. For this purpose, nubbins of S. pistillata were maintained for six months at two pHTs (8.1 and 7.2, by bubbling seawater with CO2). The lowest pH value was used to tackle how seawater pH impacts the carbon budget of a scleractinian coral. Rates of photosynthesis and respiration of the symbiotic association and of isolated symbionts were assessed at each pH. The fate of 13C photosynthates was then followed in the symbionts and the coral host for 48 h. Nubbins maintained at pHT 7.2 presented a lower areal symbiont concentration, and lower areal rates of gross photosynthesis and carbon incorporation compared to nubbins maintained at pHT 8.1. The total carbon acquisition was thus lower under low pH. However, the total percentage of carbon translocated to the host as well as the amount of carbon translocated per symbiont cell were significantly higher under pHT 7.2 than under pHT 8.1 (70% at pHT 7.2 vs. 60% at pHT 8.1), such that the total amount of photosynthetic carbon received by the coral host was equivalent under both pHs (5.5 to 6.1 µg C/cm**2/h). Although the carbon budget of the host was unchanged, symbionts acquired less carbon for their own needs (0.6 compared to 1.8 µg C/cm**2/h), explaining the overall decrease in symbiont concentration at low pH. In the long term, such decrease in symbiont concentration might severely affect the carbon budget of the symbiotic association.

Effects of cyanide on coral photosynthesis: implications for identifying the cause of coral bleaching and for assessing the environmental effects of cyanide fishing

Modulated chlorophyll fluorescence techniques were used to examine the effects of cyanide (NaCN) from cyanide fishing on photosynthesis of the symbiotic algae (zooxanthellae) located within the tissues of the zooxanthellate hard coral Plesiastrea versipora. Incubating corals for 3 h in a cyanide concentration of >10(-5) M NaCN under a saturating light intensity (photosynthetically active radiation [PAR] intensity of 250 mu mol quanta m(-2) s(-1)) caused a long-term decrease in the ratio of variable to maximal fluorescence (dark-adapted F-v/F-m). The effect of cyanide on dark-adapted F-v/F-m was Light dependent; thus F-v/F-m only decreased in corals exposed to 10(-4) M NaCN for 3 h under PAR of 250 mu mol quanta m(-2) s(-1). In corals where dark-adapted F-v/F-m was significantly lowered by cyanide exposure, we observed significant loss of zooxanthellae from the tissues. causing the corals to discolour (bleach). To further examine the light-dependent effect of cyanide and its relation to loss of zooxanthellae, corals were exposed to 10-4 M NaCN or seawater only (control), either in darkness or under 250 mu mol quanta m(-2) s(-1). ill significant decrease in dark-adapted F-v/F-m and loss of zooxanthellae only occurred in corals exposed to cyanide in the light. These results suggest cyanide causes the dissociation of the symbiosis (bleaching) by affecting photosynthesis of the zooxanthellae. Quenching analysis using the saturation-pulse technique revealed the development of high levels of non-photochemical quenching in cyanide-exposed coral. This result is consistent with the known property of cyanide as an inhibitor of the dark reactions of the Calvin cycle, specifically as an inhibitor of ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco). Therefore, chronic photoinhibition and an impairment of photosynthesis of zooxanthellae provides an important 'signal' to examine the environmental effects of cyanide fishing during controlled releases in situ.

Genetic variability of the symbiotic dinoflagellates from the wide ranging coral species Seriatopora hystrix and Acropora longicyathus in the Indo-West Pacific

The scleractinian coral species, Seriatopora hystrix and Acropora longicyathus, are widely distributed throughout the latitudinal range of the tropical west Pacific. These 2 coral species live in a mutually beneficial relation with symbiotic dinoflagellates (zooxanthellae), which are passed to their progeny by vertical transmission (zooxanthellate eggs or larvae) and horizontal transmission (eggs or larvae that acquire symbionts from the environment), respectively. For S. hystrix, vertical transmission might create biogeographically isolated and genetically differentiated symbiont populations because the extent of its larval migration is known to be limited. On the other hand, horizontal transmission in corals such as A. longicyathus may result in genetically connected symbiont populations, especially if its zooxanthellae taxa are widely distributed. To examine these hypotheses, symbionts were collected from colonies of S. hystrix and A. longicyathus living in the Great Barrier Reef (Australia), South China Sea (Malaysia) and East China Sea (Ryukyus Archipelago, Japan), and were examined using restriction fragment length polymorphism and sequence analysis of large and small subunit rRNA genes. Phylogenetic analysis assigned the symbionts to 1 of 3 taxonomically distinct groups, known as clades. Symbionts from Australian and Japanese S. hystrix were placed in Clade C, and Malaysian S. hystrix symbionts in the newly described Clade D. Seven of 11 Australian and all Japanese and Malaysian colonies of A. longicyathus had symbiotic dinoflagellates that also grouped with Clade C, but symbionts from the remaining Australian colonies of A. longicyathus grouped with Clade A. Analysis of molecular variance of Clade C symbionts found significant genetic variation in 1 or more geographic groups (69.8%) and to a lesser extent among populations within geographic regions (13.6%). All populations of Clade C symbionts from S. hystrix were genetically differentiated according to geographic region. Although Clade C symbionts of A. longicyathus from Japan resolved into a distinct geographic group, those from Australia and Malaysia did not and were genetically connected. We propose that these patterns of genetic connectivity correlate with differences in the dispersal range of the coral or symbiont propagules and are associated with their respective modes of symbiont transmission.

ENCORE: The effect of nutrient enrichment on coral reefs. Synthesis of results and conclusions

Coral reef degradation resulting from nutrient enrichment of coastal waters is of increasing global concern. Although effects of nutrients on coral reef organisms have been demonstrated in the laboratory, there is little direct evidence of nutrient effects on coral reef biota in situ. The ENCORE experiment investigated responses of coral reef organisms and processes to controlled additions of dissolved inorganic nitrogen (N) and/or phosphorus (P) on an offshore reef(One Tree Island) at the southern end of the Great Barrier Reef, Australia. A multi-disciplinary team assessed a variety of factors focusing on nutrient dynamics and biotic responses. A controlled and replicated experiment was conducted over two years using twelve small patch reefs ponded at low tide by a coral rim. Treatments included three control reefs (no nutrient addition) and three + N reefs (NH4Cl added), three + P reefs (KH2PO4 added), and three + N + P reefs. Nutrients were added as pulses at each low tide (ca twice per day) by remotely operated units. There were two phases of nutrient additions. During the initial, low-loading phase of the experiment nutrient pulses (mean dose = 11.5 muM NH4+; 2.3 muM PO4-3) rapidly declined, reaching near-background levels (mean = 0.9 muM NH4+; 0.5 muM PO4-3) within 2-3 h. A variety of biotic processes, assessed over a year during this initial nutrient loading phase, were not significantly affected, with the exception of coral reproduction, which was affected in all nutrient treatments. In Acropora longicyathus and A. aspera, fewer successfully developed embryos were formed, and in A. longicyathus fertilization rates and lipid levels decreased. In the second, high-loading, phase of ENCORE an increased nutrient dosage (mean dose = 36.2 muM NH4+; 5.1 muM PO4-3 declining to means of 11.3 muM NH4+ and 2.4 muM PO4-3 at the end of low tide) was used for a further year, and a variety of significant biotic responses occurred. Encrusting algae incorporated virtually none of the added nutrients. Organisms containing endosymbiotic zooxanthellae (corals and giant clams) assimilated dissolved nutrients rapidly and were responsive to added nutrients. Coral mortality, not detected during the initial low-loading phase, became evident with increased nutrient dosage, particularly in Pocillopora damicornis. Nitrogen additions stunted coral growth, and phosphorus additions had a variable effect. Coral calcification rate and linear extension increased in the presence of added phosphorus but skeletal density was reduced, making corals more susceptible to breakage. Settlement of all coral larvae was reduced in nitrogen treatments, yet settlement of larvae from brooded species was enhanced in phosphorus treatments. Recruitment of stomatopods, benthic crustaceans living in coral rubble, was reduced in nitrogen and nitrogen plus phosphorus treatments. Grazing rates and reproductive effort of various fish species were not affected by the nutrient treatments. Microbial nitrogen transformations in sediments,were responsive to nutrient loading with nitrogen fixation significantly increased in phosphorus treatments and denitrification increased in all treatments to which nitrogen had been added. Rates of bioerosion and grazing showed no significant effects of added nutrients, ENCORE has shown that reef organisms and processes investigated ill situ were impacted by elevated nutrients. Impacts mere dependent on dose level, whether nitrogen and/or phosphorus mere elevated and were often species-specific. The impacts were generally sub-lethal and subtle and the treated reefs at the end of the experiment mere visually similar to control reefs. Rapid nutrient uptake indicates that nutrient concentrations alone are not adequate to assess nutrient condition of reefs. Sensitive and quantifiable biological indicators need to be developed for coral reef ecosystems. The potential bioindicators identified in ENCORE should be tested in future research on coral reef/nutrient interactions. Synergistic and cumulative effects of elevated nutrients and other environmental parameters, comparative studies of intact vs. disturbed reefs, offshore vs, inshore reefs, or the ability of a nutrient-stressed reef to respond to natural disturbances require elucidation. An expanded understanding of coral reef responses to anthropogenic impacts is necessary, particularly regarding the subtle, sub-lethal effects detected in the ENCORE studies. (C) 2001 Published by Elsevier Science Ltd.

Seawater carbonate chemistry and coral (Acropora digitifera and Acropora tenuis) algal infection rate, survival and surface area of plyps during experiments, 2009

Ocean acidification, caused by increased atmospheric carbon dioxide (CO2) concentrations, is currently an important environmental problem. It is therefore necessary to investigate the effects of ocean acidification on all life stages of a wide range of marine organisms. However, few studies have examined the effects of increased CO2 on early life stages of organisms, including corals. Using a range of pH values (pH 7.3, 7.6, and 8.0) in manipulative duplicate aquarium experiments, we have evaluated the effects of increased CO2 on early life stages (larval and polyp stages) of Acropora spp. with the aim of estimating CO2 tolerance thresholds at these stages. Larval survival rates did not differ significantly between the reduced pH and control conditions. In contrast, polyp growth and algal infection rates were significantly decreased at reduced pH levels compared to control conditions. These results suggest that future ocean acidification may lead to reduced primary polyp growth and delayed establishment of symbiosis. Stress exposure experiments using longer experimental time scales and lower levels of CO2 concentrations than those used in this study are needed to establish the threshold of CO2 emissions required to sustain coral reef ecosystems.

Major cellular and physiological impacts of ocean acidification on a reef building coral

As atmospheric levels of CO2 increase, reef-building corals are under greater stress from both increased sea surface temperatures and declining sea water pH. To date, most studies have focused on either coral bleaching due to warming oceans or declining calcification due to decreasing oceanic carbonate ion concentrations. Here, through the use of physiology measurements and cDNA microarrays, we show that changes in pH and ocean chemistry consistent with two scenarios put forward by the Intergovernmental Panel on Climate Change (IPCC) drive major changes in gene expression, respiration, photosynthesis and symbiosis of the coral, Acropora millepora, before affects on biomineralisation are apparent at the phenotype level. Under high CO2 conditions corals at the phenotype level lost over half their Symbiodinium populations, and had a decrease in both photosynthesis and respiration. Changes in gene expression were consistent with metabolic suppression, an increase in oxidative stress, apoptosis and symbiont loss. Other expression patterns demonstrate upregulation of membrane transporters, as well as the regulation of genes involved in membrane cytoskeletal interactions and cytoskeletal remodeling. These widespread changes in gene expression emphasize the need to expand future studies of ocean acidification to include a wider spectrum of cellular processes, many of which may occur before impacts on calcification.

Ocean acidification rapidly reduces dinitrogen fixation associated with the hermatypic coral Seriatopora hystrix

Since productivity and growth of coral-associated dinoflagellate algae is nitrogen (N)-limited, dinitrogen (N2) fixation by coral-associated microbes is likely crucial for maintaining the coral-dinoflagellate symbiosis. It is thus essential to understand the effects future climate change will have on N2 fixation by the coral holobiont. This laboratory study is the first to investigate short-term effects of ocean acidification on N2 fixation activity associated with the tropical, hermatypic coral Seriatopora hystrix using the acetylene reduction assay in combination with calcification measurements. Findings reveal that simulated ocean acidification ( pCO2 1080 µatm) caused a rapid and significant decrease (53%) in N2 fixation rates associated with S. hystrix compared to the present day scenario ( pCO2 486 µatm). In addition, N2 fixation associated with the coral holobiont showed a positive exponential relationship with its calcification rates. This suggests that even small declines in calcification rates of hermatypic corals under high CO2 conditions may result in decreased N2 fixation activity, since these 2 processes may compete for energy in the coral holobiont. Ultimately, an intensified N limitation in combination with a decline in skeletal growth may trigger a negative feedback loop on coral productivity exacerbating the negative long-term effects of ocean acidification.

The future of coral reefs

Coral reefs, with their millions of species, have changed profoundly because of the effects of people, and will continue to do so for the foreseeable future. Reefs are subject to many of the same processes that affect other human-dominated ecosystems, but some special features merit emphasis: (i) Many dominant reef builders spawn eggs and sperm into the water column, where fertilization occurs. They are thus particularly vulnerable to Allee effects, including potential extinction associated with chronic reproductive failure. (ii) The corals likely to be most resistant to the effects of habitat degradation are small, short-lived “weedy” corals that have limited dispersal capabilities at the larval stage. Habitat degradation, together with habitat fragmentation, will therefore lead to the establishment of genetically isolated clusters of inbreeding corals. (iii) Increases in average sea temperatures by as little as 1°C, a likely result of global climate change, can cause coral “bleaching” (the breakdown of coral–algal symbiosis), changes in symbiont communities, and coral death. (iv) The activities of people near reefs increase both fishing pressure and nutrient inputs. In general, these processes favor more rapidly growing competitors, often fleshy seaweeds, and may also result in explosions of predator populations. (v) Combinations of stress appear to be associated with threshold responses and ecological surprises, including devastating pathogen outbreaks. (vi) The fossil record suggests that corals as a group are more likely to suffer extinctions than some of the groups that associate with them, whose habitat requirements may be less stringent.

Coral reefs in a century of rapid environmental change

Coral reefs are the most diverse marine ecosystem and embrace possibly millions of plant, animal and protist species. Mutualistic symbioses are a fundamental feature of coral reefs that have been used to explain their structure, biodiversity and existence. Complex inter-relationships between hosts, habitats and symbionts belie closely coupled nutrient and community dynamics that create the circumstances for something from nothing (or the oasis in a nutrient desert). The flip side of these dynamics is a close dependency between species, which results in a series of non-linear relationships as conditions change. These responses are being highlighted as anthropogenic influences increase across the world's tropical and subtropical coastlines. Caribbean as well as Indo-Pacific coral populations are now in a serious decline in many parts of the world. This has resulted in a significant reorganization of how coral reef ecosystems function. Among the spectra of changes brought about by humans is rapid climate change. Mass coral bleaching - the loss of the dinoflagellate symbionts from reef-building corals - and mortality has affected the world's coral reefs with increasing frequency and intensity since the late 1970s. Mass bleaching events, which often cover thousands of square kilometres of coral reefs, are triggered by small increases (+1-3degreesC) in water temperature. These increases in sea temperature are often seen during warm phase weather conditions (e.g. ENSO) and are increasing in size and magnitude. The loss of living coral cover (e.g. 16% globally in 1998, an exceptionally warm year) is resulting in an as yet unspecified reduction in the abundance of a myriad of other species. Projections from general circulation models (GCM) used to project changes in global temperature indicate that conditions even under the mildest greenhouse gas emission scenarios may exceed the thermal tolerances of most reef-building coral communities. Research must now explore key issues such as the extent to which the thermal tolerances of corals and their symbionts are dynamic if bleaching and disease are linked; how the loss of high densities of reef-building coral will affect other dependent species; and, how the loss of coral populations will affect the millions of people globally who depend on coral reefs for their daily survival.

Cell death and degeneration in the symbiotic dinoflagellates of the coral Stylophora pistillata during bleaching

Rising sea temperatures are increasing the incidences of mass coral bleaching (the dissociation of the coral-algal symbiosis) and coral mortality. In this study, the effects of bleaching (induced by elevated light and temperature) on the condition of symbiotic dinoflagellates (Symbiodinium sp.) within the tissue of the hard coral Stylophora pistillata (Esper) were assessed using a suite of techniques. Bleaching of S. pistillata was accompanied by declines in the maximum potential quantum yield of photosynthesis (F-v/F-m, measured using pulse amplitude modulated [PAM] fluorometry), an increase in the number of Sytox-green-stained algae (indicating compromised algal membrane integrity and cell death), an increase in 2',7'-dichlorodihydrofluroscein diacetate (H(2)DCFDA)stained algae (indicating increased oxidative stress), as well as ultrastructural changes (vacuolisation, losses of chlorophyll, and an increase in accumulation bodies). Algae expelled from S. pistillata exhibited a complete disorganisation of cellular contents; expelled cells contained only amorphous material. In situ samples taken during a natural mass coral bleaching event on the Great Barrier Reef in February 2002 also revealed a high number of Sytox-labelled algae cells in symbio. Dinoflagellate degeneration during bleaching seems to be similar to the changes resulting from senescence-phase cell death in cultured algae. These data support a role for oxidative stress in the mechanism of coral bleaching and highlight the importance of algal degeneration during the bleaching of a reef coral.

Global assessment of coral bleaching and required rates of adaptation under climate change

Elevated ocean temperatures can cause coral bleaching, the loss of colour from reef-building corals because of a breakdown of the symbiosis with the dinoflagellate Symbiodinium. Recent studies have warned that global climate change could increase the frequency of coral bleaching and threaten the long-term viability of coral reefs. These assertions are based on projecting the coarse output from atmosphere-ocean general circulation models (GCMs) to the local conditions around representative coral reefs. Here, we conduct the first comprehensive global assessment of coral bleaching under climate change by adapting the NOAA Coral Reef Watch bleaching prediction method to the output of a low- and high-climate sensitivity GCM. First, we develop and test algorithms for predicting mass coral bleaching with GCM-resolution sea surface temperatures for thousands of coral reefs, using a global coral reef map and 1985-2002 bleaching prediction data. We then use the algorithms to determine the frequency of coral bleaching and required thermal adaptation by corals and their endosymbionts under two different emissions scenarios. The results indicate that bleaching could become an annual or biannual event for the vast majority of the world's coral reefs in the next 30-50 years without an increase in thermal tolerance of 0.2-1.0 degrees C per decade. The geographic variability in required thermal adaptation found in each model and emissions scenario suggests that coral reefs in some regions, like Micronesia and western Polynesia, may be particularly vulnerable to climate change. Advances in modelling and monitoring will refine the forecast for individual reefs, but this assessment concludes that the global prognosis is unlikely to change without an accelerated effort to stabilize atmospheric greenhouse gas concentrations.

Tolerance of endolithic algae to elevated temperature and light in the coral Montipora monasteriata from the southern Great Barrier Reef

Photosynthetic endolithic algae and cyanobacteria live within the skeletons of many scleractinians. Under normal conditions, less than 5% of the photosynthetically active radiation (PAR) reaches the green endolithic algae because of the absorbance of light by the endosymbiotic dinoflagellates and the carbonate skeleton. When corals bleach (loose dinoflagellate symbionts), however, the tissue of the corals become highly transparent and photosynthetic microendoliths may be exposed to high levels of both thermal and solar stress. This study explores the consequence of these combined stresses on the phototrophic endoliths inhabiting the skeleton of Montipora monasteriata, growing at Heron Island, on the southern Great Barrier Reef. Endoliths that were exposed to sun after tissue removal were by far more susceptible to thermal photoinhibition and photo-damage than endoliths under coral tissue that contained high concentrations of brown dinoflagellate symbionts. While temperature or light alone did not result in decreased photosynthetic efficiency of the endoliths, combined thermal and solar stress caused a major decrease and delayed recovery. Endoliths protected under intact tissue recovered rapidly and photoacclimated soon after exposure to elevated sea temperatures. Endoliths under naturally occurring bleached tissue of M. monasteriata colonies (bleaching event in March 2004 at Heron Island) acclimated to increased irradiance as the brown symbionts disappeared. We suggest that two major factors determine the outcome of thermal bleaching to the endolith community. The first is the microhabitat and light levels under which a coral grows, and the second is the susceptibility of the coral-dinoflagellates symbiosis to thermal stress. More resistant corals may take longer to bleach allowing endoliths time to acclimate to a new light environment. This in turn may have implications for coral survival.

The evolutionary history of Symbiodinium and scleractinian hosts - Symbiosis, diversity, and the effect of climate change

Marine invertebrates representing at least five phyla are symbiotic with dinoflagellates from the genus Symbiodinium. This group of single-celled protists was once considered to be a single pandemic species, Symbiodinium microadriaticum. Molecular investigations over the past 25 years have revealed, however, that Symbiodinium is a diverse group of organisms with at least eight (A-H) divergent clades that in turn contain multiple molecular subclade types. The diversity within this genus may subsequently determine the response of corals to normal and stressful conditions, leading to the proposal that the symbiosis may impart unusually rapid adaptation to environmental change by the metazoan host. These questions have added importance due to the critical challenges that corals and the reefs they build face as a consequence of current rapid climate change. This review outlines our current understanding of the diverse genus Symbiodinium and explores the ability of this genus and its symbioses to adapt to rapid environmental change. (c) 2006 Rubel Foundation, ETH Zurich. Published by Elsevier GmbH. All rights reserved.

Why are there so few genetic markers available for coral population analyses?

Coral reefs are in serious decline, and research in support of reef management objectives is urgently needed. Reef connectivity analyses have been highlighted as one of the major future research avenues necessary for implementing effective management initiatives for coral reefs. Despite the number of new molecular genetic tools and the wealth of information that is now available for population-level processes in many marine disciplines, scleractinian coral population genetic information remains surprisingly limited. Here we examine the technical problems and approaches used, address the reasons contributing to this delay in understanding, and discuss the future of coral population marker development. Considerable resources are needed to target the immediate development of an array of relevant genetic markers coupled with the rapid production of management focused data in order to help conserve our globally threatened coral reef resources.